Mar Biol (2011) 158:2695–2703 DOI 10.1007/s00227-011-1767-7

ORIGINAL PAPER

Functional effects of the hadal sea cucumber Elpidia atakama (Echinodermata: Holothuroidea, Elasipodida) reflect small-scale patterns of resource availability

A. J. Jamieson • A. Gebruk • T. Fujii • M. Solan

Received: 19 May 2011 / Accepted: 27 July 2011 / Published online: 7 August 2011 Ó Springer-Verlag 2011

Abstract Holothuroidea represent the dominant benthic terms of abundance and biomass (Rice et al. 1982; Ohta megafauna in hadal trenches (*6,000–11,000 m), but little 1983; Sibuet 1985; Billett 1991). A consistent feature of is known about their behaviour and functional role at such holothurian communities, irrespective of location, is the depths. Using a time-lapse camera at 8,074 m in the Peru– marked increase in diversity at abyssal depths (3,000– Chile Trench (SE Pacific Ocean), we provide the first in 6,000 m) (Billett 1991) relative to bathyal (1,000–3,000 m) situ observations of locomotory activity for the elasipodid (Hansen 1975) and hadal depths ([6,000 m) (Hansen 1957; holothurian Elpidia atakama Belyaev in Shirshov Inst Belyaev 1989). Frequently observed mass abundances of Oceanol 92:326–367, (1971). Time-lapse sequences reveal holothurians, particularly in trenches associated with high ‘run and mill’ behaviour whereby bouts of feeding activity productivity in temperate and sub-Antarctic latitudes, have are interspersed by periods of locomotion. Over the total led some authors to refer to the hadal zone as ‘‘the kingdom of observation period (20 h 25 min), we observed a mean Holothuroidea’’ (sensu Belyaev 1989), a view that has been (±SD) locomotion speed of 7.0 ± 5.7 BL h-1, but this reinforced by trawl-catch frequencies of 88% at depths increased to 10.9 ± 7.2 BL h-1 during active relocation [6,000 m (comparable only to Polychaeta) and high levels and reduced to 4.8 ± 2.9 BL h-1 during feeding. These of dominance (75–98% in number of all organisms retrieved, observations show E. atakama translocates and processes [90% biomass) at depths [7,500 m (Belyaev 1989). sediment at rates comparable to shallower species despite Although such high returns tend to be associated with trawls extreme hydrostatic pressure and remoteness from surface- confined to the bottom of the axial part of the trenches, where derived food. the greatest quantity of organic matter accumulates (Otosaka and Noriki 2000; Danovaro et al. 2003; De Leo et al. 2010; Jamieson et al. 2010), it follows that the cumulative contri- Introduction bution of the Holothuroidea to deep ocean benthic process and functioning must be considerable (Amaro et al. 2010). Deposit feeding invertebrates, such as the Holothuroidea, Despite such high levels of abundance, intra- and inter- dominate benthic megafaunal communities in the deep sea in specific competition is thought to be low because indi- vidual species of holothurians adopt different feeding strategies, including preferential feeding on nutritionally Communicated by S. Uthicke. rich patches (Hauksson 1979; Hudson et al. 2005) and/or subtle differences in mobility or feeding behaviour & A. J. Jamieson ( ) T. Fujii M. Solan (Hudson et al. 2005; Godbold et al. 2009) that allow them Oceanlab, Institute of Biological and Environmental Sciences, University of Aberdeen, Main Street, Newburgh, to utilise different fractions of the same detrital food Aberdeenshire AB41 6AA, UK source (Uthicke and Karez 1999; Miller et al. 2000). It is e-mail: [email protected] also known that differences in feeding rates (compare, for example, Hudson et al. 2005; Godbold et al. 2009) alter A. Gebruk P.P. Shirshov Institute of Oceanology, Russian Academy the gut residence time of a food parcel, leading to more of Sciences, Nakhimovsky Pr. 36, Moscow 117997, Russia efficient digestion and rates of assimilation (Hiratsuka and 123 2696 Mar Biol (2011) 158:2695–2703

Uehara 2007). Whilst these physiological and behavioural (Echevin et al. 2008), a region of high surface productivity adaptations influence holothurian activity, much of the (averaging 269 g C m-2 year-1, Longhurst et al. 1995) ingested material is of low nutritional value (Lopez and with values reported as high as 3,613 g C m-2 year-1 Levinton 1987), leading to foraging activity that results in (Fossing et al. 1995). significant levels of surficial bioturbation that has seldom been quantified (Sibuet and Lawrence 1981; Bett and Rice 1993; Uthicke 1999; Roberts et al. 2000; Bett et al. 2001). Equipment Indeed, a recent review of invertebrate bioturbation (Teal et al. 2008) indicates a paucity of such data from bathyal We deployed Hadal-lander B (Jamieson et al. 2009b), a or abyssal depths (maximum depth data obtained = free-falling lander equipped with a 5 megapixel digital still 5,654 m, Yang et al. 1986) and a complete absence of camera (OE14-208; Kongsberg Maritime, UK) and a information from hadal depths. Hence, it is clear that the Conductivity, Temperature and Depth (CTD) sensor (SBE- ecological consequences of particle redistribution follow- 19plus V2; SeaBird Electronic Inc. USA), at 8,074 m in the 0 ing holothurian foraging and feeding activities are not Richards Deep, Peru–Chile trench (23° 22.470 S, 71° 0 known despite the importance of this group in deep ocean 19.973 W) on the 13 September 2010. The camera was mounted vertically (altitude 1 m) providing a visible area ecosystems. -2 In contrast to shallower environments, where species of 62 9 46.5 cm (0.29 m ). We attached a bait (*1kg can be caught and returned to the laboratory, carrying out of Tuna, Thunnus sp.) to a 1-cm-diameter scaled bar in the controlled experimental manipulations on hadal specimens centre of the field of view (FOV) and positioned to inter- is difficult. Direct in situ experimental manipulations are sect the sediment–water interface. Time-lapse images were possible using remotely operated vehicles (ROVs), but taken at 60-s intervals. The CTD probe recorded temper- progress is slow as there is only one vehicle capable of ature (°C), salinity, and pressure (dbar) every 10 s. Lander sampling [6,000 m (Fletcher et al. 2010). A more prac- recover was achieved by acoustically jettisoning ballast tical solution is the use of free-fall baited cameras weights to initiate the ascent to the surface. CTD data were (Jamieson et al. 2009a, b) which allow time-lapse or averaged, and pressure was converted to depth (m) continuous video recordings of benthic faunal behaviour. following Saunders (1981). Here, we use such technology to present the first detailed in situ account of the locomotion and feeding behaviour of Image analysis the holothurian Elpidia atakama (Belyaev 1971) (family Elpidiidae) at 8,074 m in the Richards Deep area of the Motion paths of E. atakama were tracked using ImageJ Peru–Chile trench. This species has never been seen alive 1.42q, a Java-based public domain program developed at and appears to be endemic to the Peru–Chile trench. We the USA National Institutes of Health (available at, compare locomotion speed and feeding behaviour with http://rsb.info.nih.gov/ij/index.html). Images were cali- abyssal analogues and conclude that the observed patterns brated and analysed in chronological order. We used the of activity are consistent with the view that the behaviour X–Y coordinates at the base of the central feeding tentacle of E. atakama reflects exploitation of patchily distributed as a location marker and calculated the distance (cm) an resources. We contend that the ability to exploit envi- individual travelled per time step to determine the absolute locomotion speed (cm h-1) as follows: ronmental heterogeneity in this way explains, at least in qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi part, why the holothurians are so abundant and outcom- 2 2 d ðÞX2 X1 þ ðÞY2 Y1 pete other deposit feeding species at abyssal and hadal a ¼ ¼ ð1Þ depths. t t where a˜ = absolute locomotion speed, cm h-1; d = dis- tance, cm; and t = time interval (here, 60 s). We also explore how differences in time-lapse interval Materials and methods alter ecological interpretation by re-calculating the absolute locomotion speed (and percentage deviation in error rela- Study site tive to the highest resolution of observation) for E. atakama at 1-, 2-, 5-, 10-, 20- and 60-min intervals and place our The Peru–Chile Trench (SE Pacific Ocean) is the longest results within the context of other findings published in the trench in the world (5,900 km 9 100 km, Angel 1982) and scientific literature. runs parallel to the west coast of South America from In order to account for body size, we divided a˜ by body Ecuador to central Chile. The trench lies below the length (BL = longest axis of specimen) to provide a size- Humboldt Current and the Peruvian upwelling system specific speed (BL h-1). 123 Mar Biol (2011) 158:2695–2703 2697

Results these together, a˜ = 35.5 ± 29.3 cm h-1 (7.0 ± 5.7 BL h-1), giving a mean swept area rate (a˜ 9 body width 9 We recorded 1,225 images (20 h 25 min) at a calculated distance/t) of 81.6 cm-2 h-1. The speed and direction of depth of 8,072 m (=8,276 dbar). At this depth, water movement was neither constant nor unidirectional (Fig. 2), temperature was 2.25°C and salinity was 34.68. Sequences reflecting a ‘run and mill’ movement pattern (Kaufmann included observations of the holothurian, Elpidia atakama, and Smith 1997), i.e. relatively large distances are achieved and three species of scavenging gammarid amphipods: with minimal changes in speed and direction (routine Eurythenes gryllus, (Thurston et al. 2002), Hirondellea locomotion) and are interspersed with bouts of localised, sp.nov. (Perrone et al. 2002) and an unidentified species. closely spaced turns that allow sediment processing and After 20 h, the bait remained present but had been signif- feeding (milling activity, sensu Smith et al. 1993; Fig. 2). icantly reduced by scavenging amphipods (Fig. 1). Closer examination of our images suggests that feeding E. atakama was observed (starting at 48 min elapsed does not take place during routine locomotion (all feeding time) on three occasions (Period A, 218 images or 3 h tentacles protrude forward clear of the sediment–water 38 min; Period B, 138 images or 2 h 18 min; and Period C, interface), rather feeding tentacles only contact the sedi- 219 images or 3 h 44 min; total = 9 h 40 min; Fig. 1), ment–water interface during milling activity (Fig. 3). This which were separated by periods of time when the indi- demarcation of behaviour alters the locomotion ability of vidual moved out of the field of view (2 h 18 min and the organism and leads to temporally distinct activity 20 min, respectively). Within these sequences, the number periods. For example, following its first appearance (Period of images in which E. atakama was present varied, A), E. atakama exhibited a locomotion speed of ranging from 76 images (1 h 16 min) in Period B, 140 59.3 cm h-1 for 26 min (11.6 BL h-1) before it began a images (2 h 20 min) in Period A, to 203 images (3 h bout of feeding (or milling) activity for 55 min in a 23 min) in Period C. The individual was not always fully localised area, characterised by irregular but short-distance visible within the field of view; hence, only images where movements at 17.4 cm h-1 (3.4 BL h-1). On the cessation the head was clearly visible were used to track holothurian of any obvious feeding activity, locomotion speed increased activity. We matched exit to entrance positions between to 61.7 cm h-1 (12.1 BL h-1) for 53 min before feeding sequences and checked body size measurements (*5.1 9 started again at a speed of 15.4 cm h-1 (3.0 BL h-1) for 2.3 cm) and confirmed that all appearances were the same 6 min. Similar observations were also observed in the individual. second period (Period B), where E. atakama fed for The distance that E. atakama traversed varied over time, the first 49 min at a speed of 23.0 cm h-1 (4.5 BL h-1) but the rate of movement did not appear to be related to the before relocating at a speed of 43.6 cm h-1 (8.5 BL h-1) length of time the individual was observed. Maximal for 27 min until exiting the field of view. In the third locomotion speed was attained during Period A (96.5 cm in appearance (Period C), E. atakama fed for the majority of 140 min, = 41.36 cm h-1 or 8.1 BL h-1), with lower time (152 min) with two small periods of routine move- rates of movement observed in Periods B (37.3 cm in ments (31 and 20 min). The locomotion speed during bouts 76 min, = 29.45 cm h-1 or 5.8 BL h-1) and C (133 cm in of relocation was 54.0 cm h-1 (10.6 BL h-1), but during 203 m, = 33.6 cm h-1 or 6.6 BL h-1). When averaging feeding, reduced to 27.1 cm h-1 (5.3 BL h-1). In total,

Fig. 1 a Full field of view image from 8,075 m showing the tuna bait parcel in the centre with four scavenging amphipods (Eurythenes gryllus) beginning to feed. In the centre, middle is the holothurian Elpidia atakama. b Close-up of E. atakama. Scales bars = 5cm 123 2698 Mar Biol (2011) 158:2695–2703

Fig. 2 Absolute speed (cm min-1) over time and the X–Y track for the three appearances of E. atakama (a, b, c). Periods of feeding (milling) activity are shaded. Trend lines are 10 min moving averages. In the right hand panels, S marks the start position and E the end position

E. atakama spent 150 min relocating and 267 min feeding to make given the lack of available data and differences in (a ratio of 1:1.8). By distinguishing between routine methodology (Fig. 5). Re-analysis of our own data showed locomotion and feeding locomotion, mean locomotive that increasing the time-lapse interval over the observation speeds were 55.7 ± 36.7 cm h-1 (10.9 ± 7.2 BL h-1) and period results in a rapid (logarithmic) increase in error, 24.3 ± 14.8 cm h-1 (4.77 ± 2.9 cm h-1), respectively. resulting in[55% estimate error when images are taken at It is important to place the current observations within 60-min intervals (decreases from 7.0 ± 5.7 BL h-1 to the context of other known observations of holothurian 3.2 ± 0.9 BL h-1; Fig. 5a), relative to the highest resolu- behaviour (Table 1). Whilst it is clear that the rate of tion of observations (1 min). Data using 60-min intervals locomotion in E. atakama is faster than many other species, from Kaufmann and Smith (1997) and Smith et al. (1993) these differences relate only poorly to increasing depth and 1-min intervals from (Smith et al. 1997) are in good (Fig. 4a) or to body size (Fig. 4b). An alternative expla- agreement with our predictions (Fig. 5b). Furthermore, the nation may be that the rate of locomotion relates to the measurements of the rate of movement of Elpidia minu- quality and reliability of food supply, although this tissima (Smith et al. 1993; Kaufmann and Smith 1997) are hypothesis has not been tested explicitly and we almost equal to those of E. atakama based on a theoretical acknowledge that comparisons between studies are difficult 60-min interval.

123 Mar Biol (2011) 158:2695–2703 2699

Fig. 3 The a locomotion and b feeding behaviour of E. atakama. locomotion and b lowered to intersect the sediment–water interface Feeding tentacles are a positioned to the anterior (the bottom of each during bout of feeding. Frames were selected at random from image) and raised above the sediment–water interface during successive bouts of locomotion and feeding

Table 1 Summary of measured body length (BL), absolute (a˜) and size-specific locomotion speeds for holothurians at a range of depths Species Depth (m) BL (cm) a˜ (cm h-1) Size-specific Source speed (BL h-1)

Laetmogone violacea 1,000 14.0 102.6 7.3 Smith et al. (1997) Benthogone rosea 2,012–2,019 17.0 89.0 5.0 Billett (1991) Staurocucmuis abyssorum 4,100 12.9 12.8 1.0 Kaufmann and Smith (1997) Staurocucumis abyssorum 4,100 9.7 17.8 1.8 Smith et al. (1993) Elpidia minutissima 4,100 4.4 11.9 2.7 Kaufmann and Smith (1997) Elpidia minutissima 4,100 4.1 14.8 3.6 Smith et al. (1993) Peniagone vitrea 4,100 8.6 10.1 1.2 Kaufmann and Smith (1997) Peniagone vitrea 4,100 7.3 8.1 1.1 Smith et al. (1993) Scotoplanes globosa 4,100 9.5 16.3 1.7 Kaufmann and Smith (1997) Synallactes profundi 4,100 17.4 12.7 0.7 Kaufmann and Smith (1997) Oneirophanta mutabilis 4,100 15.3 64.6 4.2 Kaufmann and Smith (1997) Oneirophanta mutabilis 4,100 14.3 84.8 5.9 Smith et al. (1993) Oneirophanta mutabilis 4,844 16.2 128.9 8.0 Smith et al. (1997) Elpidia atakama 8,074 5.1 37.3 7.3 Present study

Discussion (Smith et al. 1993; Kaufmann and Smith 1997), and locomotion and feeding rates are comparable to holothu- We have documented the feeding and locomotion behav- rians found at shallower depths. However, our findings iour of a hadal holothurian and shown that the behaviour is provide compelling evidence that E. atakama is a func- not exceptional; the run and mill pattern of Elpidia atak- tionally important species that is likely to change its ama exemplifies patterns of behaviour of functionally behaviour in response to localised resource heterogeneity analogous abyssal species in the NE Pacific, including (Godbold et al. 2009, 2011) and the repackaging of organic Elpidia minutisima, Staurocucumis abyssorum, Synallac- matter (OM; Bett et al. 2001). Also, movement over the tes profundi, Peniagone vitrea and Scotoplanes globosa sediment surface associated with relocation constitutes

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Fig. 4 Summary of observations of size-specific locomotion speed (BL h-1) for a water column depth and b body size of individual holothurians. Open circles represent measurements for E. atakama in the present study, whilst closed circles represent the data listed in Table 1

Fig. 5 The effect of increasing the elapsed time between successive 60-min time-lapse intervals (recalculated from present study data) time-lapse images on mean locomotion speeds for the holothurians alongside previously published data (triangles) for the abyssal species listed in Table 1.Ina, the degree of estimation error increases rapidly listed in Table 1. Estimates for E. minutissima are denoted by grey as time-lapse intervals are extended (recalculated from present study circles data). In b, data are shown for E. atakama at 1-, 2-, 5-, 10-, 30-, and bioturbation which is qualitatively distinct from bioturba- Belyaev 1989). In general, however, the density of the tion associated with feeding activity (Bulling et al. 2008), Elpidiidae family (Elpidia glacialis ushakovi, E. glacialis giving credence to the view that epifaunal species can have solomonensis, Elipida sp., Peniagone purpurea, P. azorica a substantial effect on the properties of the sediment profile and Scotoplanes globosa) at hadal depths can range from (Solan et al. 2004). It is, however, difficult to assess the 0.5 to 10 ind. m-2 (5,000–100,000 ind. ha-1) (Lemche ecological contribution of E. atakama in the absence of et al. 1976). More recent reports from the Orkney trench information on the spatial extent and temporal persistence (Vinogradova et al. 1993; Gebruk 1993) suggest for of this species. There are no abundance estimates for E. decapoda, a density of 15 ind. m-2 (150,000 ind. ha-1) E. atakama (or any other holothurian) in the Peru–Chile at 6,160 m and 30 ind. m-2 (300,000 ind. ha-1) at 5,580 m. Trench. However, a review of all-known hadal records up These estimates are considerably higher than those repor- to 1989 found that the density of both E. uschakovi in the ted for the abyssal plains; most reports indicate 15.5–193.3 New Hebrides trench and Elpidia sp. from the Palau trench ind. ha-1, although there are some exceptions, e.g. 370.8 was 0.1 ind. m-2 (=1,000 ind. ha-1), whilst the density of ind. ha-1, E. minutissima in the NE Pacific (Kaufmann and E. solomonensis from the New Britain and Bougainville Smith 1997) and in the NE Atlantic, 8.77–337.92 ind. ha-1 Trenches ranged from 0.03 to 0.1 and 0.01 ind. m-2, for Amperima rosea, and 43,949 ind. ha-1 for Elpidia respectively (300–1,000 ind. ha-1 and 100 ind. ha-1; echinata, although there are instances of mass occurrences

123 Mar Biol (2011) 158:2695–2703 2701 of Kolga hyaline at 501,701 ind. ha-1 (Billett and influence species contributions to ecosystem properties at Hansen 1982; Billett 1991; Billett et al. 2001). Never- much larger scales (Godbold et al. 2011). theless, using the calculated sweep area and observations Whilst we have been able to describe the likely ecolog- of feeding activity obtained here, we estimate that a ical role of E. atakama at hadal depths, the high-resolution single individual of E. atakama may process 1 m2 of time-lapse sequences also enabled us to highlight some surficial sediment every 5.1 days, or a population of 123 procedural difficulties that are likely to hinder progress in individuals will turnover 1 m2 of surficial sediment every understanding the structure and functioning of hadal com- hour. munities (Jamieson et al. 2010). Reanalysis of our time- When considered together, the available estimates of lapse sequences at progressively lower temporal resolution holothurian density provide anecdotal evidence that holo- suggests that the extended time-lapse intervals used in long- thurians are found in greatest abundance at hadal depths, term observatories (Kaufmann and Smith 1997) are likely to rather than at adjacent abyssal areas. Mass abundances of miss the subtleties of holothurian behaviour and grossly hadal holothurians are thought to occur at the trench axis underestimate the locomotion/feeding rates of individual where elevated levels of organic material are likely to species, because rest periods and alternative bouts of accumulate (Otosaka and Noriki 2000; Danovaro et al. behaviour can occur between successive images (typically 2003; Jamieson et al. 2010; Itoh et al. 2011). This appears \1 h). This source of error makes pairwise comparisons to reflect a general relationship with topography (Rowe between different studies, locations or seasons difficult and 1971) as concentrations of elpidiids are a common feature hinders generic understanding of ecological phenomena of underwater canyons and other depressions which are (Benton et al. 2007). If we are to fully appreciate the known to contain elevated levels of organic matter and functional role of organisms that inhabit the deepest parts of deposit feeding benthic biomass (De Leo et al. 2010). It has our oceans, extended observations are now needed that been shown that density of benthic assemblages in trenches appreciate the temporal and spatial scales at which species- tends to be related positively to productivity in surface environment interactions occur and which aim to test waters: highest densities in trenches that occur at high unambiguously ecological theory. latitudes and/or close to continents (Belyaev 1989). Whilst it is tempting to speculate that the behaviour we have Acknowledgments Supported by the HADEEP project (Nippon observed here is a response to the spatio-temporal vari- Foundation, Japan, and the Natural Environmental Research Council, UK). We thank the chief scientist Prof. Hans-Joachim Wagner ability in the extent and intensity of food supply (Ruhl (University of Tu¨bingen, Germany) and the crew of the RV Sonne 2007; Smith et al. 2009), the study region is eutrophic, and SO209. We thank Dr. Niamh Kilgallen (National Institute for Water food resources are plentiful, albeit complicated by inter- and Atmosphere research, New Zealand) and Dr. Kota Kitazawa annual phenomena of the region, including the El Nino (Atmosphere and Ocean Research Institute, University of Tokyo, Japan) for their assistance at sea. AJJ is currently supported by the Southern Oscillation and the development of oxygen Marine Alliance for Science and Technology Scotland (MASTS). minimum zones (Thiel et al. 2007). Furthermore, inter- annual and seasonal variation in abundances of abyssal holothurians is known to occur (Billett et al. 2001, 2010; References Ruhl 2007; Smith et al. 2009) and will also be likely at hadal depths. Under these circumstances, it is unlikely that Amaro T, Bianchelli S, Billett DSM, Cunha MR, Pusceddu A, competition for resources will lead to behavioural differ- Danovaro R (2010) The trophic biology of the holothurian Molpadia musculus ences in feeding strategy (Godbold et al. 2009). In the : implications for organic matter cycling and ecosystem functioning in a deep submarine canyon. Biogeo- present study, E. atakama spent 150 min relocating and sciences 7:2419–2432 267 min feeding (a ratio of 1:1.8), suggesting that resource Angel MV (1982) Ocean trench conservation. International union for supply is indeed abundant and that the distance between conservation of nature and natural resources. Environmentalist patches is relatively short (20–40 min travel time, or 2:1–17 Belyaev GM (1971) Deep water holothurians of the genus Elpidia. approximately 10 body length distance). This pattern of Transactions of P. P. Shirshov Inst Oceanol 92:326–367 movement suggests considerable sensitivity to food con- Belyaev GM (1989) Deep-Sea Ocean trenches and their fauna. Nauka centration (McClintic et al. 2008) and implies that the Publishing House, Moscow, p 385 (Translated to English from dynamics and organisation of hadal communities are inti- Russian by Scripps Institution of Oceanography, USA, 2004) Benton TG, Solan M, Travis J, Sait SM (2007) Microcosm mately linked to habitat structure and the distribution of experiments can inform global ecological problems. 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